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doi: 10.1111/j.1365-2664.2009.01713.x
Conservation implications of rainforest use patterns: mature forests provide more resources but secondary forests supply more medicine
Michael C. Gavin*
School of Geography, Environment and Earth Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand
Summary 1. Tropical rainforests are a global conservation priority. Robust arguments supporting rainforest conservation can attract funding and shape land-use management. However, some popular assertions regarding the value of tropical forests remain largely untested. 2. This study tests the validity of two arguments in support of mature tropical rainforest conservation: rst, that these forests should be conserved based on their value as potential sources of medicine. This argument requires mature forests to be better sources of medicine than alternative land-use types, including secondary forests. Second, secondary forest use may help conserve mature forests by providing sucient resources to buer against resource extraction in mature forests. 3. The research was conducted in three communities in the Cordillera Azul, Peru, where 369 individuals from 66 households were surveyed. Participants recorded all ora and fauna collected in mature (>20 years) and secondary forests over 180 days in six use categories (food, medicine, wood, weavings, adornments and other). Ecological knowledge of secondary and mature forest species was assessed for male and female household heads. 4. Households used 346 folk species (as dened by local classication systems) from 3668 collection events. Individuals had better knowledge of secondary forest species, but more access to mature forests. Participants collected signicantly more medicines from secondary than from mature forests. In other major use categories (food, wood, weaving, adornment), secondary forests provided fewer resources than mature forests. Participants collected a dierent set of species from secondary and mature forests, with only 130 folk species (38%) collected in both secondary and mature forests. 5. Synthesis and applications. The arguments to protect mature rainforests as sources of new drugs may be overstated, because secondary forests can provide more medicinal plant resources than mature forests, and landscapes that incorporate forests of dierent ages can maximize availability of medicinal plant species. Conservation eorts must take a landscape level approach given the spread of resource use across dierent forest types. Because of the heterogeneity of resource availability and use among community members, and the dynamic nature of resource use on forest frontiers, conservation should embrace participatory adaptive management approaches that incorporate a variety of resource users. Key-words: Amazon, conservation planning, ethnobiology, forest option value, medicine, natural resource use, pharmaceutical bioprospecting, secondary forests, tropical rainforests
Introduction
Tropical rainforests are a global conservation priority. Numerous arguments have been formulated in support of conserva-
tion of these forests. Here, the validity of two such arguments are tested: one based on the potential value of mature rainforests as sources of pharmaceuticals, and the other focused on use of secondary forests as a buer against extraction in older forests. The idea that we must protect mature tropical rainforests as possible sources of new medicines gained popularity in the 1980s and 1990s buoyed by academic research and the
1276 M. C. Gavin popular press, and supported by the Convention on Biological Diversity (Hamilton 2004; Voeks 2004; Burtis 2007). Tropical rainforests contain at least two-thirds of the planets terrestrial biodiversity, and more plant species than any other biome (Mittermeier et al. 1999; Kier et al. 2005; Gardner et al. 2009). Therefore, these ecosystems have been portrayed as ideal hunting grounds for new drugs. Mendelsohn & Balick (1995) note that 47 pharmaceuticals have been developed from rainforest plant extracts, and they estimate that an additional 328 remain to be discovered. The total revenue from these discoveries could total $32$47 billion, and would increase to $147 billion if social benets of the medicines are calculated (Mendelsohn & Balick 1995). Other estimates of the option value of rainforests for drug discovery range up to $18 trillion (Principe 1991; Gentry 1993; Pearce & Puroshothaman 1995). However, the expected windfall from bioprospecting has been tempered by a recent shift in the pharmaceutical industry towards laboratory-based drug discovery (Macilwain 1998; Firn 2003). In addition, in most cases, the few prots bioprospecting has brought have not beneted conservation (Laird & ten Kate 2002; Hamilton 2004; Burtis 2007). Despite these setbacks, several researchers are still optimistic that scientic advances can improve the eciency of bioprospecting, and that improved regulations can ensure benets are equitably shared with conservation receiving more funding (e.g. Rausser & Small 2000; Laird & ten Kate 2002; Kursar et al. 2006, 2007; Ragavan 2008). Arguments in support of bioprospecting can point to the fact that over one-third of new medicines have been derived from natural sources since the early 1980s (Newman, Cragg & Snader 2003; Koehn & Carter 2005). However, an important ecological caveat is fundamental to the option value argument: for mature tropical forests to be conserved based on potential medicinal value, they should be better sources of medicine than alternative land-use types, including secondary forests. Secondary forests are also the focus of another conservation strategy. Tropical mature forests are a critical source of natural resources for millions of people across the globe (Sunderlin et al. 2005). This widespread use of forest products has had enormous impacts on mature rainforest ecosystems, including habitat loss and extirpation of targeted species (Redford 1992; FAO 2007). If sucient forest products can be found on other land-use types, some of the pressure on mature forests may be relieved. This is an increasingly relevant strategy as tropical landscapes become mosaics of dierent uses. Mature rainforests are progressively more fragmented due to the spread of pasture lands, agriculture, and logging (FAO 2007). Historically, these disturbed lands have been written o in terms of their value for biodiversity conservation (Vandermeer & Perfecto 2007; Chazdon et al. 2009). However, these landscapes are not mere wastelands, but often comprise complex patchworks, including tracts of secondary forests at various stages of ecological succession that can hold impressive amounts of biodiversity and provide critical ecological services and products (Tschakert, Coomes & Potvin 2007; Harvey et al. 2008; Gardner et al. 2009). These secondary forests derive both from the dynamics of swidden-fallow agriculture, in which crop plots are rotated to allow nutrient recovery, and from land abandoned as market forces change livelihoods (e.g. shifts away from extensive pasture use) or lead to immigration to urban centres (Rudel, Bates & Machinguiashi 2002). Due to this combination of forest clearance and fallowing or abandonment, tropical secondary forests are some of the fastest expanding resources on the planet. If secondary forests can provide sucient natural resources, extraction from mature forests may diminish (Brown & Lugo 1990; Chazdon & Coe 1999; Robinson & Bennett 2004; FAO 2005). As Robinson & Bennett (2004) note, the use of secondary forests may allow us the opportunity to have our wildlife (and plants) and eat it too. This conservation strategy requires secondary forests to provide sucient resources to serve as alternatives to mature forest extraction. In this study, both the medicinal option value argument and the secondary forest extraction alternative are tested by examining the use of plants and animals by local communities in the Cordillera Azul region of the Peruvian Amazon.
2009 The Author. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology, 46, 12751282
Results
Ecological knowledge varied signicantly based on origins of heads of household, sex and domain of knowledge (animals vs. plants). In both forest types, indigenous heads of households (n = 105) had higher levels of ecological knowledge than immigrants (n = 27, P < 0001). Men (n = 66) scored better on ecological knowledge in both forest types than women (n = 66; P < 0001). In both forest types, heads of household also had better knowledge of animals than of plants (n = 132; P < 0001). However, in general, regardless of origins, sex or domain of knowledge, heads of household (n = 132) had better knowledge of secondary forest species (Median = 75% questions correct) than mature forest species (Median = 50%; P < 0001; see Fig. 1). Participants recorded a total of 3668 collection events, in which they used 346 dierent folk species. The 66 households surveyed extracted 130 folk species from both mature and secondary forests, 105 folk species only from mature forests, and 111 from only secondary forests. Participants used more folk species from mature forests for wood, weavings, adornments, and other uses; but for food, mature forests (108 folk species) and secondary forests (109 folk species) were the sources of approximately the same number of species (Fig. 2a). Medicine was the only use category in which households extracted notably more species from secondary forests (83 folk species, 58 of which were unique to secondary forests) than from mature forests (52 folk species, 27 of which were unique to mature
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(a)
10 Secondary forest knowledge Mature forest knowledge 08
Ecological knowledge (% correct answers)
(a) 60
No. of folk spp. used
50 40 30 20 10 0
Collected in mature forest only Collected in mature and secondary Collected in secondary forest only
06
04
Food
(b) 1000
Meds
Wood
Weave
Adorn.
Other
02
Mature forest
Amazonia
(b)
10
400
200
08
0
06
Food
Meds
Wood
Weave
Adorn. Other
Fig. 2. Number of folk species (a) and number of collection events (b) from secondary and mature forests collected for dierent uses by 66 households in Cordillera Azul, Peru.
04
*
02
Men
Women
Fig. 1. Box plots of mature and secondary forest ecological knowledge of (a) local vs. immigrant and (b) male vs. female heads of household (n = 132) in the Cordillera Azul, Peru.
forests). In total, more collection events occurred in mature forests (2036) than in secondary forests (1632), and mature forests saw more collection events for every use category except medicine and other (Fig. 2b). The summaries of species used and collection events for all 66 households mask the great variability in use within the sample (see Fig. 3). For example, the number of folk species collected by individual households ranged from 0 to 63 in mature forests and 1 to 46 in secondary forests. Collection events ranged from 0 to 92 in mature forests and 1 to 101 in secondary forests. Households collected more resources in mature forests (Median = 29 collection events) than in secondary forests (Median = 21) (P < 005). Importantly, results varied for dierent use categories (Fig. 3a): For food (P < 005), wood (P = 0001), and adornments (P < 0001) more collection events occurred in mature forests. I found no signicant dierence in collection events between forest types for weaving materials or other uses. However, for medicine more collection events occurred in secondary (Median = 5) than in mature forests (Median = 3, P < 0001). Even when I con-
trolled for origins of household heads (i.e. indigenous vs. immigrant, data not shown), medicine is the only use category with more collection events in secondary forests. Regardless of family origins, medicine is also the only use category with signicantly more species extracted from secondary forests (Fig. 3b). Households used more folk species from mature forests for food (P < 005), wood (P < 0001), and adornments (P < 0001). I found no dierence in the number of folk species used from dierent forest types for weaving or other uses. However, for medicines, participating households extracted signicantly more folk species from secondary forests (Median = 4) than from mature forests (Median = 2, P < 0001). The types of folk species extracted from secondary and mature forests also varied (Table 1). Participating households collected nearly one-third (111) of folk species used from just one forest type. Of the fty most collected plants and animals in each forest type, only 17 were collected in both secondary and mature forests. Twenty animal folk species were in the top 50 most collected folk species in mature forests, but only 10 animal folk species made the top 50 list in secondary forests. Animal collection events accounted for 47% of all mature forest collection, but only 22% of secondary forest collection. Whereas palms (Arecaceae) were the most widely collected family of plants in both forest types, the top ve most collected plant folk species were dierent between the two forest types. For animal species, two species (Dasyprocta fuliginosa and Agouti paca) were in the top ve most collected in both forest types.
2009 The Author. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology, 46, 12751282
10
1 01 1
10 More secondary forest collection 100 Food Meds. Wood Weave Adorn. Other
(b)
More mature forest collection Safe Log (difference in no. spp. used) 10
1 01 1
number of collection events a household made in secondary vs. mature forests (adjusted R2 02 for all use categories). In addition, the folk forest classication (i.e. mature forests dened as over 20 years old) has a potentially large inuence over the results. Ecologically-based classications of forest types may identify forests as secondary well beyond 20 years following disturbance, based on species compositions and forest structure. Such a shift in the timeframe used to dene secondary forests could alter some of my conclusions (i.e. even more species and collection events may be in secondary forests). Because ecological surveys or detailed land-use histories were not available for each plot of land where resource use occurred, I cannot be certain that all forests over 20 years old were undisturbed in the past. However, the nature of local land tenure arrangements mean that most forests over 20 years old in the communities sampled have probably been undisturbed by humans for a considerable time period, and would thus be called mature even under ecological classication systems. Because of the quantity of open-access land in the region, in most cases, families claimed new parcels of land that had been undisturbed prior to their working on them. In turn, only in cases where families had worked on a parcel for more than 20 years (n = 4, 6% of cases) would the possibility exist that mature forest had been disturbed by humans in the recent past. The results presented here did not dier when these four households were removed from the analysis.
Discussion
Other
Food
Meds.
Wood
Weave
Adorn.
Fig. 3. Box plots indicating the dierence in number of collection events (a) and number of species collected (b) between secondary and mature forests across dierent use categories for 66 dierent households in the Cordillera Azul, Peru. (Note: negative values indicate more species used or more collection events in secondary forests, and positive values indicate more in mature forests. Safe log allows for use of 0 and negative values. Safe log = sign(x) log(1 + abs(x)).
Comparisons between secondary and mature forest collection may be inuenced by the relative availability of the forest types. The households surveyed had much more mature forest available to them. Mature forest covered virtually all openaccess lands outside of the agricultural zones of the communities surveyed. In addition, participants owned far more mature forest (Median = 26 ha, 73% of total holding) than secondary forest (Median = 388 ha, 16% of total holding, P < 0001). However, the proportion of secondary forest on private holdings varied widely (084%). Despite this large range in availability, neither the amount of secondary forest owned nor the proportion of land in secondary forests was a good predictor of the relative number of folk species a household used from secondary vs. mature forests (across all use categories linear regressions had adjusted R2 02). Similarly, neither the amount of secondary forest owned nor the proportion of land in secondary forests was able to predict the relative
Although popular conservation arguments hold that mature forests should be conserved for their high potential medicinal value and that mature forests might be conserved by encouraging local use of secondary forests, the results presented here imply the opposite conclusions. Previous studies point to the potential value of disturbed habitats (including secondary forests) as sources of medicinal plants (e.g. Toledo et al. 1992; Frei, Sticher & Heinrich 2000; Stepp & Moerman 2001). For example, seven healers interviewed by Voeks (1996) in Brazil identied more potentially useful medicinal plants in secondary forests than in primary forests. Similarly, Posey (1984) found Kayapo informants believed 94% of species encountered in secondary forests were potentially useful for medicine, whereas almost no species in primary forest had potential for medicine. In this study, the actual use of plants and animals in the Cordillera Azul was recorded, and it was found that informants collected more medicinal plant folk species and undertook more medicinal plant collection events in secondary forests. Based on these results, secondary forests may have greater option value for medicinal prospecting than mature forests. However, because the ethnobotanical survey method used here focused only on locally useful species, some mature forest species (e.g. canopy epiphytes in mature forests), and the secondary compounds they hold, are certainly underrepresented. Two factors hypothesized as contributing to the importance of disturbed habitats for medicinal plant collection are accessibility and familiarity. Recent studies noted that species which
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Table 1. Most frequently collected species and families in mature and secondary forests in the Cordillera Azul, Peru (n = 369 resource users) Collection events Collection events
Secondary forest Ten most collected plant families Arecaceae Ulmaceae Bombacaceae Fabaceae Cyclanthaceae Euphorbiaceae Sterculiaceae Rubiaceae Rutaceae Verbenaceae Five most collected plant folk species Atadijo Trema micrantha (L.) Blum. Bombonaje Carludovica palmata Ru z & Pav. Shapaja Attalea butyracea (Mart. Ex L. f.) Weis Topa Ochroma pyramidale (Cav. ex Lam.) Urb. Sangre de grado Croton lechleri Muell. Arg. Five most collected animal folk species An uje Dasyprocta fuliginosa Conejo Sylvilagus brasiliensis Majas Agouti paca Zorro Didelphis marsupialis Carachupa Bombero Dasypus kappleri
Mature forest
111 94 80 75 73 69 64 51 48 48 94 73 62 51 42 63 35 25 25 18
Arecaceae Meliaceae Fabaceae Araceae Moraceae Rubiaceae Bignoniaceae Bombacaceae Celastraceae Euphorbiaceae Shapaja Attalea butyracea (Mart. Ex L. f.) Weis Tamshi Heteropsis sp. Caoba Swietenia macrophylla Piesaba Geonoma sp. Chuchuhuasi Maytenus sp. An uje Dasyprocta fuliginosa Venado Colorado Mazama americana Majas Agouti paca Sajino Tayassu tajacu Pucacunga Penelope spp.
are relatively more abundant or available (e.g. due to seasonal constraints), may be used more frequently (Albuquerque 2006; Lucena, Lima Araujo & Albuquerque 2007). Secondary forests are often more accessible to local people given the predominance of these forests in human-dominated landscapes (Voeks 1996, 2004; Stepp & Moerman 2001). However, accessibility does not appear to be a crucial factor in determining sources of medicinal plants in communities surveyed in this study in the Cordillera Azul because households had access to more mature forests. Likewise, the proportion of land held in secondary forest was not a good predictor of the relative use of secondary forests. Alternatively, local people may be more familiar with secondary forest species (Voeks 2004). Support was found for this hypothesis in the Cordillera Azul, with both indigenous and non-indigenous heads of households holding more ecological knowledge related to secondary forests. Although some medicinal plants can be found in mature forests, the ethnobotanical survey method used here leads to the conclusion that secondary forests are the source of more medicinal plants than mature forests; and a landscape with a mixture of secondary and mature forests would maximize medicinal plant availability. Critical to this argument is the nature of secondary forests. Not all secondary forests are created equally. The number of species secondary forests contain, as well as forest structure, ecosystem functions, and forest product availability will vary based on numerous factors, including the level of disturbance prior to succession, degree of isolation from seed sources, and the degree of management intervention during forest recovery (cf. Chazdon 2008 and references therein). Therefore, the managed fallows in the Cordillera Azul will be likely to contain far more species than other
secondary forest types, such as commercial plantations. However, if some secondary forests, such as those studied here, are just as good or better sources of medicinal plants than mature forests, then conservation arguments based on the value of mature forests for bioprospecting will need to be rethought. For instance, in the Cordillera Azul, biodiversity values may be maximized by conserving large stands of mature forests, but bioprospecting values could be maximized with land that supports a mix of mature and secondary forests. Although the households I surveyed had higher levels of ecological knowledge of secondary forest species, they still preferred mature forests for collection in use categories other than medicine. Under current livelihood strategies, secondary forests cannot buer against mature forest extraction. Local people can be expected to collect products that best match their needs. Overall, in the Cordillera Azul, mature forests provided more products, in terms of total collection events. However, in general, resource use in the two forest types appeared to be complementary. Participating families collected dierent folk species in mature vs. secondary forests (see Table 1). Secondary forests also seem unlikely to serve as alternative sources for many resources given that mature forests were the sole source of 105 folk species, many of which are mature forest obligates. In terms of use categories, secondary forests produced more useful medicine; whereas mature forests, that harbour larger trees, were better sources of wood products. Therefore, because current livelihood strategies require local people to access both secondary and mature forests, land management in the Cordillera Azul, whether focused on conservation or on local development, will need to be done on a landscape scale. This conclusion mirrors similar recommendations from other
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Conservation implications of rainforest use 1281 social-ecological systems in tropical forests (e.g. Harvey et al. 2008; Chazdon et al. 2009; Gardner et al. 2009). Conservation eorts centred on mature forests in the region (e.g. Cordillera Azul National Park) cannot aord to design management in isolation of the surrounding human-dominated matrix. This point is even more pertinent given the dynamic nature of the human-dominated landscapes, in which mature forests are rapidly converted into other land uses. Any conservation conclusions reached by studies of current resource use patterns must reect the dynamic social and ecological landscape of forest frontiers. The relative coverage of dierent forest types and the use of these forests vary greatly within communities. For example, the number of mature forest folk species used in the communities studied here varied from 1 to 46, and the hectares of secondary forest owned ranged from 084% of total land owned. Other studies from the Peruvian Amazon report similar heterogeneity in land ownership and resource use (e.g. Takasaki, Barham & Coomes 2001; Tschakert et al. 2007). This heterogeneity of resource availability and use emphasizes the need to incorporate a wide range of stakeholders into conservation processes to ensure that management can account for the needs and potential impacts of dierent resource users (Salafsky & Margoluis 2004; Gavin, Wali & Vasquez 2007). In addition, forest coverage and use will vary over time. As is true of many tropical rainforest frontiers regionally and globally (Wittemyer et al. 2008), the buer zone of the Cordillera Azul is undergoing rapid change driven by high rates of immigration. Immigrants arrive from all over Peru seeking open lands to establish farms. Immigration will probably increase forest clearance, and ultimately increase the proportion of land held in secondary forests. More secondary forest could alter livelihood strategies. Resource users could switch to use more secondary forest species, or they may seek the same mature forest species by collecting resources farther from community centres. For the communities focused on here, this would mean potentially more forest collection inside the national park. Therefore, conservation management cannot ignore local resource use outside the protected area. A participatory adaptive management approach provides the best option for incorporating the concerns and needs of local stakeholders into management, within a framework that continuously gathers new data and changes according to available information and the dynamic nature of the social-ecological system in question (Salafsky, Margoluis & Redford 2008). In fact, the Cordillera Azul National Parks management plan already includes participatory adaptive management in a landscape level approach to the management of natural resource use (Gavin, Wali & Vasquez 2007). In conclusion, the resource use patterns recorded in the Cordillera Azul have several important conservation implications. For one, arguments to protect mature rainforests as sources of new drugs may be signicantly overstated because secondary forests may provide more medicinal plant resources than mature forests, and a landscape that incorporates forest of dierent ages can maximize availability of medicinal plant species. Secondly, conservation eorts must take a landscape level approach given the impacts of resource users on dierent forest types. Thirdly, a variety of dierent resource users should be included in the management process given the heterogeneity of resource availability and use among community members. Finally, the highly dynamic nature of social-ecological systems on forest frontiers can alter resource use over time, and therefore conservation in these locations should embrace participatory adaptive management approaches.
Acknowledgements
I thank J. Solomon, R. Dunn, W. Linklater, R. Wallace, two anonymous reviewers and the editors for useful comments. Field research was supported by grants from the Conservation, Food, and Health Foundation, Switzer Foundation, US Fulbright Programs, Garden Club of America, and the Conservation and Research Foundation. I thank G. Anderson, the sta of the Centro de Conservacion, Investigacion, y Manejo de Recursos Naturales, the Centro de Desarrollo e Investigacion de la Selva Alta, the Instituto de Investigaciones de la Amazonia Peruana, M. Vasquez, M. Ozambela, and L. Garcia for invaluable assistance and advice. Special thanks to the communities who supported the research eort in countless ways.
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